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Published in final edited form as: Curr Opin Biomed Eng. 2023 Sep 3;28:100498. doi: 10.1016/j.cobme.2023.100498

Sensory Restoration for Improved Motor Control of Prostheses

Lee E Fisher 1,2,3,4,5,8, Robert A Gaunt 1,2,3,4,5, He Huang 6,7
PMCID: PMC10583965  NIHMSID: NIHMS1935684  PMID: 37860289

Abstract

Somatosensory neuroprostheses are devices with the potential to restore the senses of touch and movement from prosthetic limbs for people with limb amputation or paralysis. By electrically stimulating the peripheral or central nervous system, these devices evoke sensations that appear to emanate from the missing or insensate limb, and when paired with sensors on the prosthesis, they can improve the functionality and embodiment of the prosthesis. There have been major advances in the design of these systems over the past decade, although several important steps remain before they can achieve widespread clinical adoption outside the lab setting. Here, we provide a brief overview of somatosensory neuroprostheses and explores these hurdles and potential next steps towards clinical translation.

1. Introduction

Somatosensation from the hands and feet is crucial to effortlessly and skillfully perform most activities of daily living. Sensory input from our hands enables us to modulate grip force, shape our grasp around objects, and track the locations of our fingers, especially when vision is obstructed [1]. Somatosensation from the legs, and especially the soles of the feet, is critical for maintaining balance and responding to postural perturbations [2]. For both the arms and legs, somatosensation also allows us to embody our limbs and experience them as being connected to our bodies and belonging to us [3]. Injuries such as limb amputation and spinal cord injury disrupt or damage somatosensation, and without this feedback, even the most advanced prosthetic limbs remain extracorporeal tools that require visual feedback and substantial attentional effort to achieve even basic control. For example, in upper-limb prosthetics, near-constant visual attention is required to maintain hand position and grip force [4], and in lower-limb prosthetics, impaired somatosensation is associated with an increased rate of falls [5].

Over the past decade, substantial investments of time and research dollars have been focused on developing implantable clinical neuroprostheses (Figure 1) to restore somatosensation from the limbs to improve control of prosthetic devices. This is actually a resurgence in interest, as there was a substantial focus on restoring sensation to amputees in the 1970s and 1980s, including investigations of a fully-implantable stimulator [6] and an extensive historical review of these technologies [7]. The initial goal of recent studies was to demonstrate that electrical stimulation of spared somatosensory pathways with implanted electrodes could produce sensations that appeared to emanate from the amputated or paralyzed limb [8–10]. The primary focus of these studies were to understand the location and perceptual qualities (e.g., intensity, discriminability, modality) of sensations evoked by electrical stimulation [11]. As such, research teams demonstrated that it is possible to evoke sensations in the missing or paralyzed limb by stimulating the brain, spinal cord, or peripheral nerve using devices that span the spectrum from microelectrode arrays inserted into the brain to cuff electrodes wrapped around peripheral nerves [12–15]. While there are differences in the stimulation thresholds and focality of evoked sensations across these different approaches, there have also been remarkable similarities in the quality of evoked sensations, regardless of the location of stimulation, type of device used to deliver stimulation, or time since injury. Most research participants report experiencing paresthetic sensations (i.e. electrical buzzing) but almost never report proprioceptive sensations [9,13,14,16,17]. Still, these results established the feasibility of using electrical stimulation to restore somatosensation after limb amputation and laid the foundation for developing clinical systems to improve the functionality of prostheses. For detailed reviews of these studies, see [18–20].

Figure 1.

Figure 1.

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Examples of sensory-enabled prosthetic hands. (a) A bi-directional brain computer interface used for control of a robotic arm in a person with tetraplegia. Electrodes were implanted in primary motor cortex (blue) to record neural signals to control the robotic arm, and stimulation was delivered by electrodes in primary somatosensory cortex (red) to provide sensory feedback from the robotic limb. Adapted from [12]. (b) A somatosensory neuroprosthesis in which somatosensory feedback was delivered by electrical stimulation of the cervical spinal cord and the prosthetic hand was controlled by electromyographic signals recorded from muscles in the residual forearm. Stimulation amplitude was modulated by pressure signals recorded from the prosthetic fingers while the participant performed an object discrimination task. Adapted from [21].

Beyond reporting the location and quality of evoked sensations, these early studies also provided simple demonstrations that restored somatosensory feedback could be used during motor control of a limb [8]. For example, multiple studies examined tasks that cannot be performed without somatosensory feedback, such as using a prosthesis to classify object compliance and size without visual feedback [8,21]. Other studies provided practical demonstrations that users could perform challenging tasks that required dexterous control of the limb, such as removing the stem from a cherry without crushing the fruit [9]. Additional studies characterized participants’ speed and ability when performing simple clinical tasks of function, such as the Action Research Arm Test (for upper-limb function) or the Sensory Organization Test (for lower-limb function) [22,23].

The rapid progress over the past decade has laid the scientific foundation and demonstrated the clinical feasibility of many new somatosensory neuroprostheses. However, if these devices and approaches are to achieve broad clinical adoption, we must transition from demonstrations of feasibility to larger studies in real-world environments. In this opinion article, we describe barriers and propose next steps towards broad clinical translation of somatosensory neuroprostheses. We describe the surprising similarity in evoked sensations regardless of the anatomical target of stimulation and discuss techniques to potentially enhance the modality and quality of those sensations. We also identify independent development of sensory and motor neuroprostheses as a barrier to implementation of a complete closed-loop system and propose that future studies should focus on co-development of these systems. Finally, we propose the need to focus on studies involving long-term use outside the lab to demonstrate the effect of restored somatosensation on motor control. These barriers are certainly not easy to overcome, and the solutions will require multidisciplinary collaboration, but by addressing them, we believe the field will make important strides towards widespread clinical adoption of somatosensory neuroprostheses.

2. Neural interfaces and targets for somatosensory restoration

Anatomical targets

The anatomical targets for human somatosensory neural interfaces have expanded considerably in the last decade. The first somatosensory neuroprostheses were developed to restore sensation to amputees and typically used vibro- or electro-tactile stimulation of the skin on the residual limb [24]. This was soon followed by electrical stimulation of peripheral nerves using implanted electrodes [6]. For recent reviews on sensory restoration in amputees see [1,25,26]. While studies of non-invasive systems continue [27], most recent efforts have focused on implantable peripheral nerve interfaces with electrodes placed on (i.e., epineural) [9,28] or within (i.e., extrafascicular or intrafascicular) [8,29,30] the nerve. These peripheral nerve electrodes activate primary afferent axons that remain intact after amputation and have been repeatedly shown to evoke sensations that are referred to the missing limb, even decades after amputation [6,10]. Epidural spinal cord stimulation (SCS) has also been used to evoke sensations from the phantom limbs of amputees [13] by activating the same primary afferents that are stimulated with peripheral nerve stimulation, albeit, in a different location. One major attraction of epidural SCS is the mature clinical market for treating pain that could allow rapid translation, given that as many as 50,000 SCS systems are implanted every year in the United States to treat pain [31]. Ascending the somatosensory neuraxis, studies have demonstrated that electrical stimulation of the ventroposterior nucleus of the thalamus evokes somatosensory percepts [32], although these trials have always been performed as part of surgical procedures for other clinical indications. Similarly, one recent study demonstrated that stimulation of somatosensory cortex through clinical stereoencephalography depth electrodes could evoke sensations in the hand in two people with intractable epilepsy [33]. Lastly, brain-computer interfaces (BCIs) that have often focused on restoring motor function have been enhanced using implants in the somatosensory cortex that create distinct percepts across the hand and arm [12] and also improve prosthesis control [22].

Projected fields

Driven by requirements of the various anatomical targets, many different implantable electrode technologies have been developed. This is particularly true for the peripheral nerve which includes single- and multi-channel nerve cuffs that wrap around the epineural surface, as well as multielectrode arrays that penetrate the nerve [34]. To a first approximation, it is reasonable to believe that large electrodes on the epineural, spinal epidural, or cortical surface would evoke somatosensory percepts with projected fields that are referred to larger areas of the skin compared to microelectrodes implanted within the nerve or cortex. These microelectrodes could activate fewer individual neurons per electrode, thus increasing spatial resolution and ability to create different percept qualities. For example, epidural SCS evokes sensations from multiple fingers [13]. Epineural nerve cuffs [9] or cortical surface electrodes [35,36] often reduce this projected field area to the level of individual digits or portions thereof.

Intraneural [29] and intracortical [12] electrodes may further reduce these projected field sizes, depending on the location of the projected field on the body surface. However, this is not always true. While direct evaluations of the projected field sizes between extraneural and intraneural electrodes have not been done, it is often true that they are very similar to each other [8,9,16,37].

One direct driver of projected field size may be the specific region of the skin that the sensations is referred to. For example, intracortical microstimulation in a region of the cortex that represents the fingertips can evoke sensations that have projected fields that are measured in a few square millimeters, while these same electrodes placed in the palmar area of the hand evoke sensations that are square centimeters in size [38]. This is likely related to the amount of cortical territory devoted to the fingertips compared to the palm [39].

Quality

One surprising aspect of different approaches to restoring somatosensory percepts is that, to date, there is little evidence suggesting that percept quality (i.e., modality, naturalness) is affected by the anatomical location or electrode design. Electrical stimulation, delivered more peripherally, might lead to more natural – or at least interpretable – percepts, as the entire supraspinal sensory and perceptual apparatus (dorsal column nuclei, thalamus, primary and secondary somatosensory cortices, prefrontal cortex, etc.) can be engaged. Conversely, intracortical microstimulation typically only activates one specific region of the somatosensory system, such as area 1 [12]. Further, this area is more anatomically complex than the peripheral nerve. However, nearly all reports of the qualitative nature of electrical stimulation include descriptions of ‘paresthesia’, ‘tingle’, ‘buzzing’, ‘electrical stimulation’, as well as ‘vibration’, ‘touch’, and ‘pressure,’ including studies of epineural stimulation [6,9], intrafascicular stimulation [14], epidural SCS [13], thalamic stimulation [32], cortical surface stimulation [35], and intracortical stimulation [12]. At present, there seem to be no systematic differences, based on location or stimulation technology, that substantially biases percept quality to be more or less natural. Further, few studies have reported reliable proprioceptive percepts. For cortical stimulation in area 1, which is an entirely cutaneous region, this makes sense. However, in the peripheral nerve, where proprioceptive afferents are abundant, the reasons for the dominance of cutaneous percepts are unclear. While some studies have reported movement-like sensations evoked directly by electrical stimulation [29,40], in other cases, sensory substitution has been used to convey proprioceptive information [17,41,42], and in other cases residual muscle proprioception has been exploited [43].

Encoding strategies

While stimulation location and technology may not be a primary determinant of sensory quality, there is some evidence that stimulation encoding strategies may be a broadly useful method to manipulate quality. In the peripheral nerve, adopting biomimetic stimulation strategies can increase the perceived naturalness of stimulation [44] and improve task performance [29]. Preliminary evidence suggests that stimulus parameters can affect percept quality in the cortex as well [45]. Efforts to increase the accuracy of these biomimetic trains may improve sensory quality in both the peripheral and central nervous system. Regardless, any claims about the relative naturalness of stimulation through a particular anatomical target, stimulation device, or even encoding algorithm, are substantially complicated by the inherent ambiguity of the term itself and the variety of methods used to assess it. Direct comparisons of sensory qualities between participants and studies is challenging, although comparing quality differences as stimulation parameters change may be a more effective way to evaluate the effects of stimulation parameters [46]. Further, assessing the effects of any stimulation approach on task performance may be a more quantifiable, and ultimately clinically meaningful metric.

3. Development of somatosensory and motor neuroprostheses using a holistic framework

A literature search of bi-directional neuroprostheses mostly returns studies on the design of neural interfacing devices that can both stimulate and record neural signals [47–49]. In terms of clinical testing and translation of neuroprostheses, the development of motor decoding approaches for prosthesis control and encoding methods for somatosensory stimulation have been largely separated. For the design of somatosensory neuroprostheses, although studies have evaluated the effects of restored somatosensation in a closed-loop setup [1,17,21,50], the motor control scheme was typically pre-selected and did not consider the ways the somatosensory neuroprosthesis might enhance the performance of a specific motor control approach. Similarly, recent progress in the development of motor control strategies for prosthetic hands focused on developing advanced decoding algorithms to achieve dexterous control, however the sensory feedback in these studies was limited to incidental modalities (e.g., vision, pressure on the residual limb from the prosthetic socket), without also providing somatosensory feedback via a neuroprosthesis [51,52].

Because one of the primary goals of somatosensory neuroprostheses is to enhance sensorimotor integration to improve motor control, in our opinion, developing somatosensory and motor neuroprostheses should build upon an understanding of human motor control and learning theory [1,53]. Motor control theory based on internal models has been widely adopted to interpret human movement behaviors [54]. Within this control framework, the inverse model transforms the desired task goal into actions (i.e., efferent neural signals), while the forward model uses the efferent neural action (i.e., efference copy) to predict the system state. Multi-sensory feedback must be interpreted within the context of the task and environment, including task performance, limb and body state, somatosensory feedback when interacting with the environment, and reward. Together, these factors lead to the control of action and enable motor learning and updating of internal models [55,56]. When someone wears a prosthetic limb, this control framework is altered because the end effector is the prosthesis, rather than a fully integrated part of the body. Somatosensory feedback from a neuroprosthesis, the motor control scheme of the prosthesis, and the user’s internal models are connected and must operate together to achieve an optimal control system [57,58].

This design approach requires (1) an understanding of how somatosensory and motor neuroprostheses and human internal models influence each other in different task contexts, and (2) actively designing somatosensory and motor neuroprostheses within a holistic framework, considering the dynamics of each of the components and the human motor control system. A few research groups have adopted this approach to investigate how supplementary haptic interfaces influence task performance in participants using EMG-controlled prostheses [1]. For example, in one study that compared EMG-controlled grasp force scaling with and without vibro-tactile haptic feedback, researchers found that incidental feedback (such as visual feedback) was sufficient to achieve consistent task performance at low force levels, but that task performance decreased at high force levels because of the variability in the EMG signal at high contraction levels [27]. As a result, they found no improvement in task performance with the addition of haptic feedback at low force levels and only modest improvement in performance at higher force levels. However, the same group later re-designed their somatosensory feedback system to provide information about EMG signal amplitude rather than grasp force level and showed significant improvements in task performance [59]. Feedback based on the EMG signal may have directly affected the user’s internal model, facilitating the improvement in control performance. Using a similar approach, guided by motor control theory, to design next-generation somatosensory neuroprostheses may be one avenue to improve the performance of closed-loop neuroprostheses.

To our knowledge, there have been few studies that implemented a somatosensory neuroprosthesis while also studying the influence of different motor decoding schemes (continuous vs. discrete, multi-joint coordinated vs. non-coordinated, position vs. velocity vs. force control) on closed-loop task performance. Future research must also explore how different motor decoding approaches can best facilitate the effects of a somatosensory neuroprosthesis to achieve optimal motor performance.

4. Long-term trials involving community use

Assessing performance in the lab

Most studies that test the effectiveness of restored somatosensation have been performed in a lab environment under carefully controlled conditions with a variety of assessment metrics. These experiments have largely fallen into three main categories: (1) tasks that would be difficult or impossible without somatosensory feedback [8,17,21,29], (2) timed tasks in which task performance is compared with and without restored somatosensation [22,60], and (3) clinical outcome measures of function [23]. Each of these categories has been important in establishing specific benefits of restored somatosensation. For example, a common test of restored hand somatosensation involves characterizing the size and shape of objects while blindfolded [8,17,21,29,41]. Success at this task demonstrates that a participant can discriminate specific features of sensory feedback, such as the timing of stimulation onset or the rate of increase in stimulus intensity relative to grasp aperture [21]. Other studies have relied on clinical outcome measures, such as the sensory organization test, to demonstrate that restored somatosensation from the feet can reduce a participant’s reliance on visual and vestibular feedback during quiet standing [23]. These demonstrations quantify specific and important effects of restored somatosensation within the constraints of the lab environment. However, there are several challenges with these metrics. First, even studies that use a similar conceptual task (i.e., assessing object compliance, shape, size) do not use consistent objects, making it difficult to compare the results of different studies. Second, normative data typically do not exist, making it difficult to determine the real effect size of any result. To move forward, standardized tests that are appropriate for neuroprostheses must be developed and validated to enable consistent in-lab evaluations. Attempts to develop tasks that are sensitive to the effects of restored sensation are being developed [61,62], but these have not yet been broadly adopted. Ultimately though, if participants are going to truly adopt somatosensory-enabled prostheses, these devices must provide real-world improvements outside the lab.

Home-use trials

To truly understand the effects of restored sensation on the use of prosthetic and robotic devices, we must transition these experiments from the lab to the home and community. Participants must be able to use these devices in the environments where they normally use their prostheses, and we must track their long-term usage. Recently, multiple research groups have taken the first steps towards these types of studies, including take-home trials in which participants have used the systems in an unsupervised community environment [63–66]. In one study, a participant with upper-limb amputation was implanted with flat interface nerve electrodes around median and radial nerves, and was able to use the system at home for 115 days [64]. In a second study, two participants with targeted sensory reinnervation were allowed to use a bi-directional prosthesis outside the lab for up to two years [65]. In another set of studies, four participants with spiral cuff electrodes implanted around median and ulnar nerves used a bi-directional osseointegrated prosthesis for up to seven years outside the lab [28,66]. Finally, a recent case study explored the longitudinal experience of a person with transtibial amputation using a somatosensory neuroprosthesis at home for 31 weeks [67]. Critically, these studies were able to explore changes in usage and control of the devices over long periods of time while participants learned to use them, including enhanced embodiment of the limb and increased performance on functional tasks. Interestingly, the study of osseointegrated devices performed a long-term experiment which demonstrated that chronic use of a somatosensory neuroprosthesis could not remap the location of an evoked sensation from one location on the hand to another [66]. These types of results and insights are not possible unless participants can use the devices every day over long periods of time. While these experiments mark a critical first step in demonstrating the true utility of somatosensory neuroprostheses, future experiments must involve larger cohorts and should include blinding and control conditions whenever possible. This will likely require multi-site clinical trials of these systems. Further, these studies should examine the real-world effects of restored somatosensation in the most practical terms. For example, we should explore the ways in which participants continue to use sensory feedback after the initial novelty has abated and whether restored somatosensation enables performance of bimanual tasks that would otherwise require compensatory strategies. To achieve widespread clinical adoption of bi-directional neuroprostheses, we must demonstrate that the systems produce a meaningful improvement in the lives of users to justify their additional cost and complexity.

5. Conclusions

Overall, there has been substantial progress in the development of somatosensory neuroprostheses over the past decade. Across the spectrum of implanted devices, studies have demonstrated that stimulation of peripheral nerves, the spinal cord, and brain structures can evoke sensations that appear to emanate from the missing or paralyzed limb and that those sensations can enhance the control of a prosthesis. Moving forward, we believe it will be critical to carefully consider the ways that somatosensory stimulation interacts with both the target neural structures and the broader sensorimotor system. This includes designing stimulation schemes that more closely mimic the underlying neurophysiology and also implementing stimulation approaches that integrate with our understanding of motor control frameworks. Finally, to fully understand the ways people interact with these somatosensory neuroprostheses and to justify their clinical utility, it will be important to perform large-scale and longterm controlled take-home trials in which people use the devices on a daily basis outside the lab environment. We believe that these steps will facilitate clinical translation and adoption of somatosensory neuroprostheses to enhance the lives of people with limb amputation and paralysis.

Highlights.

  • Somatosensory neuroprostheses improve functionality, embodiment, and adoption of prostheses

  • Somatosensory and motor neuroprostheses are often studied independently and co-development may accelerate both systems

  • Testing of home-use of closed-loop prostheses will be critical for clinical adoption

6. Acknowledgements

The authors thank Dr. I-Chieh Lee for her valuable feedback on drafts of this manuscript. This work was supported by grants from the National Institutes of Health [UH3 NS107714, U01 NS123125, and UH3 NS100541] and the National Science Foundation [NSF 1954587, NSF 2221479].

Lee Fisher reports financial support was provided by National Institute of Neurological Disorders and Stroke. Robert Gaunt reports financial support was provided by National Institute of Neurological Disorders and Stroke. Helen Huang reports financial support was provided by National Science Foundation. Robert Gaunt is on the scientific advisory board of Neurowired LLC.

Footnotes

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7.

Declaration of Competing Interests

Robert Gaunt is on the scientific advisory boards of Neurowired LLC.

Declaration of interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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